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Larvae of Ataenius (Coleoptera: Scarabaeidae: Aphodiinae

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Larvae of Ataenius (Coleoptera: Scarabaeidae: Aphodiinae Eur. J. Entomol. 96: 57—68, 1999 ISSN 1210-5759 Larvae ofAtaenius (Coleóptera: Scarabaeidae: Aphodiinae): Generic characteristics and species descriptions José R. VERDÚ and E duardo GALANTE Departamento de Ciencias Ambientales y Recursos Naturales, Universidad de Alicante, E-03080 Alicante, Spain Key words.Scarabaeidae, Aphodiinae, Ataenius, larvae, description, key, dung beetles, turfgrass beetles, taxonomy Abstract. We compared the larval morphology of the genera Ataenius and Aphodius. The third larval instars of five Ataenius species: Ataenius opatrinus Harold, A. picinus Harold, A. platensis (Blanchard), A. simulator Harold and A. strigicauda Bates, are described or redescribed and illustrated. The most important morphological characteristics of the larvae of Ataenius are found in the respiratory plate of thoracic spiracle, the setation of venter of the last abdominal segment, the setation of the epicranial region and the morphology of the epipharynx. A key to larvae of the known species of Ataenius is included. INTRODUCTION del Sacramento (Uruguay). For the purpose of laboratory studies, a total of 10 to 20 adult specimens of each species were The genus Ataenius Harold comprises 320 species, of kept in cylindrical plastic breeding cages (20 cm high, 10 cm which 228 species are found in America, 49 in Australia, wide) with moist soil and dry cow dung from which they had 11 in Africa, 6 in East Asia, 2 in Madagascar, and single been collected. The lid was an opening (6 cm diameter) covered species in India, Sri Lanka, Turkestan, Japan, Hawaii and with gauze screen. These breeding cages were maintained in an Sumatra, respectively (Dellacasa, 1987). Despite the rich­ environmental chamber at 25 : 20°C (L : D), 80 ± 5% RH, with ness of this genus and its worldwide distribution, the lar­ a photoperiod of 15 : 9 (L : D). The breeding cages were exam­ val morphology of only 7 species is known at present ined weekly and the results recorded. Throughout the study pe­ (Jerath, 1960; Ritcher, 1966). The life historieso f Ataen­ riod, complementary data were obtained in the field. Voucher specimens are deposited in the Collection of Entomology of the ius species are not well known, but some records indicate Departamento de Ciencias Ambientales y Recursos Naturales, that they are humus- and root-feeders in soil, with a few Universidad de Alicante, Spain (C.E.U.A.). species attracted to decaying vegetation and animal dung (Wegner & Niemczyk, 1981; Ratcliffe, 1991). Some spe­ Laboratory studies cies have been captured in ant nests and animal burrows Larval specimens were fixed in KAAD solution (Carne, 1951) (Cartwright, 1974; Deloya, 1994). The trophic diversity, for 12 h and preserved in 70% ethanol. The head capsule was worldwide distribution, relative abundance [e.g., Cart­ removed from the body and both parts were placed in warm po­ tassium hydroxide for a few minutes. Finally, they were rinsed wright (1974) collected about 275,000 specimens of with distilled water and placed in glacial acetic acid for two Ataenius simulator Harold in a light trap in a single night] minutes. Dissection took place under a binocular stereo­ and the high level of fecundity (Cambefort & Hanski, microscope (magnification up to 40 x), separate parts were stud­ 1991), could explain the potential of Ataenius species as a ied in temporary slides under a microscope using magnifications pest in areas recently transformed by man, such as the of 100 and 200 x. Drawings were made using FSA 25 PE tube golf course fairways, greens and tees in the United States (Leica). The light micrographs of thoracic spiracles and tegilla (Hoffman, 1935; Aim et al., 1992). It is very important to of the last abdominal segment were recorded on Ektachrome know both the larval stages of Ataenius and the biology 64T (Kodak) film with a photomicroscope Leitz DM-RB of the species in order to pursue studies of the dynamics (Leica) using interference contrast. Distinguishing characters that are readily seen using a binocu­ of their populations (Allsopp et ah, 1995). lar microscope (magnifications of 6 to 40 x) and subject to the In this study we describe the third larval instars of five least variation were mostly selected for use in the diagnosis of Ataenius species: Ataenius opatrinus Harold, A. picinus species. Extremely minute characters were used only if neces­ Harold, A. platensis (Blanchard), A. simulator Harold and sary. Most diagnostic characteristics are found on the head and A. strigicauda Bates. The larvae of the latter three species the mouthparts and on the ventral surface of the last abdominal were described by Jerath (1960), but the lack of illustra­ segment (Ritcher, 1966; Edmonds & Halffter, 1972, 1978; Kim tions makes identification very difficult. In this paper, we & Lumaret, 1988; Verdú & Galante, 1997). The morphology of give new descriptions and anatomical illustrations of the larvae was described using anatomical terminology of Jerath larvae studied. We also provide a key to the known larvae (1960), Ritcher (1966), Kim & Lumaret (1988) and Verdú & Galante (1997). According to Ritcher (1966), when the distance of Ataenius. between the two lobes of the respiratory plate of the thoracic MATERIAL AND METHODS spiracle ranges from 100 to 80% of the dorso-ventral diameter of the bulla, “equal to or slightly less than” has been used in de­ Breeding scribing the degree of constriction; “somewhat less than” is used Parental stock was collected in July, August and September when the distance is from less than 80 to 60%; “much less than” 1995 from Castillos, Minas, San Miguel de Salinas, and Colonia 57 0.25 mm Figs 1-11: Ataenius opatrinus Harold. 1 - third instar larva, left lateral view; 2 - head, frontal view; 3 - antenna; 4 - right mandi­ ble, ventral view; 5 - right mandible, molar view; 6 - right mandible, dorsal view; 7 - left mandible, dorsal view; 8 - left mandible, molar view; 9 - left mandible, ventral view; 10 - left maxilla, dorsal view; 11- left maxilla, ventral view. Abbreviations: DES - dor- soepicranial setae; IVGS - interior ventral galea setae; LES - lateral external epicranial setae; ms - microsetae. when it is from less than 60 to 20%; and “almost contiguous” 2-4 microsetae on posterior part. Coronal suture present, when it is less than 20%. surpassing frontal suture. Clypeus transverse, on each RESULTS side one short anterior seta and one lateral seta. Labrum trilobed; on each side: one internal seta and on posterior Common morphological characteristicsof Ataenius part one long lateral seta; lateral lobe of the labrum with andAphodius larvae one seta; middle lobe of labrum with two anterior setae Body.Body arched (C-shaped) at the level of 4th or 5 th and one posterior seta. Antennae 4-segmented. Third seg­ abdominal segment (Fig. 1). ment with one ring of 5 setae and one well-developed Head. Cranium transverse, bearing on each side: one cone-shaped organ or one disc-like sensorial structure long seta on anterior frontal angle, a similar one on the (Verdu & Galante, 1997). Fourth segment short, with an lateral frontal part, one seta on anterior frontal region; a inner sensorial surface extended to dorsal and ventral posterior lateral seta on frontal region. Epicranial region: parts; apical end with one ring of sensorial setae, one minimum of two dorsoepicranial setae, 5-9 lateral setae, longer, whip-shaped. Mandibles: asymmetrical with two 58 14 0.25 mm 0.25 mm 15 Figs 12-17:Ataenius opatrinus Harold. 12 - epipharynx; 13 - hypopharynx; 14 - caudal view of last abdominal segment; 15 - raster; 16 - thoracic spiracle; 17 - palus. Abbreviations: ACP - acanthoparia; ACR - acroparia; BU - bulla; CLI - clithra; DAL - dorsal anal lobe; DX - dexiophoba; ETA - anterior epitorma; GL - glossa; LAL - lower anal lobe; LX - laeophoba; MIS - micro- sensillae; MPH - mesophoba; O - oncyli; PE - pedial area; PLA - palidium; PLG1S - posterior lateral glossae setae; PPH - proto- plioba; PTT - pternotormae; RSP - respiratory plate. or three dorso-extemal setae and two microsensilla be­ by tegumental expansion. Glossa (GL) with two pairs of tween setae. Maxilla: galea and lacinia separated. Galea macrosensilla and a transversal row of microsensilla on with two dorsolateral setae and a variable number of in­ distal part of oncyli, proximal portion with a row of setae ternal setae; ventral portion with one longitudinal row of on each side; lateral lobe with 2 pairs of setae; central internal setae. Lacinia with trilobed uncus; a microseta at lobe with 4 setae and 4 macrosensilla. the base of each lobe; one row of setae situated dorsally, Thorax.Prothorax with a dorso-lateral plate lightly with short median seta on base; one basal seta on ventral sclerotized, straw-coloured. Concavities of respiratory portion; one basal seta on uncus. Stipes with a row of plates of thoracic spiracles facing posteriorly. Legs well- stridulatory teeth; one long lateral seta; two different developed; distal portions of tarsal claws generally sized fore setae and one small lateral microseta. Maxil­ curved, with two ventral setae. lary palpus 4-jointed; first joint (palpifer) with one ventral Abdomen. Concavities of respiratory plate of abdomi­ seta; third joint with two setae; fourth joint narrowed api- nal segments facing anteriorly. Raster with teges or with cally, with sensorial longitudinal area and distal ring of definite palidia. short microsetae. Epipharynx (Fig. 12) with anterior epi­ Distinguishing morphological characteristics of torma (ETA) situated in the central pedial area (PE), pter­ Ataenius and Aphodius larvae notormae (PTT) well-sclerotized. Mesophoba (MPH) with 3 pairs of macrosensilla covered by posterior expan­ To the naked eye, Aphodius and Ataenius larvae appear sions of tegument. Dexiophoba (DX) slightly more devel­ nearly identical. Nevertheless, several characteristics dif­ oped than laeophoba (LX). Protophoba (PPH) with ferentiate the two genera. expansions of integument and a transversal row of sen- Anal lobes.In Aphodius larvae, the lower anal lobe is silla. Haptomerum with one pair of macrosensilla. Ac­ cmarginate or entire; Ataenius larvae show two lower roparia (ACR) with 4 short setae.
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